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Comparative genomics rewrites evolution textbooks: a

“postmodern synthesis” of Evolutionary Biology?

Eugene V. KooninNational Center for Biotechnology Information, NLM, NIH, Bethesda,

Maryland, USA

Moscow, Digital October, 31/10/2013

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The Modern Synthesis

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Nothing in biology makes sense except in the light of evolution

Evolutionary process represented as change in allele frequency driven by natural selection

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Haemophilus influenzae Mycoplasma genitalium

The beginnings of comparative genomes

Venter et al. 1995

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7/3/1995 7/2/1997 7/2/1999 7/1/2001 7/1/2003 6/30/2005 6/30/20071

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0%

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Most (~70-80%) of genes in prokaryotic genomes are evolutionarily conserved –belong to COGs – orthologous lineages - distinct units of evolution

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Understanding evolution in the light of comparative genomics and

systems biology: Is there a ‘postmodern synthesis’

in sight?

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Postmodern reassessment of some central propositions of Darwin and the Modern Synthesis

Proposition Postmodern status

The material for evolution is provided, primarily, by random, heritable variation (random local mutations, in modern terms).

Only partly true. The repertoire of relevant changes greatly expanded to include duplication of genes, genome regions, and entire genomes; loss of genes and, generally, genetic material; HGT including massive gene flux in cases of endosymbiosis; invasion of mobile selfish elements and recruitment of sequences from them; and more. More importantly, (quasi)directed, Lamarckian variation is recognized as a major factor of evolution.

Fixation of (rare) beneficial changes by natural selection is the main driving force of evolution.

Only partly true. Natural (positive) selection is important but is only one of several fundamental factors of evolution and is not quantitatively dominant. Neutral processes combined with purifying selection dominate evolution, and direct effects of environmental cues on the genome {(quasi)Lamarckian phenomena] are important as well.

The variations fixed by natural selection are “infinitesimally small”. Evolution adheres to gradualism.

False. Even single gene duplications and HGT of single genes are by no means “infinitesimally small” let alone deletion or acquisition of larger regions, genome rearrangements, whole-genome duplication, and most dramatically, endosymbiosis. Gradualism is not the principal regime of evolution.

Uniformitarianism: evolutionary processes remained, largely, the same throughout the evolution of life.

Only partly true. Present day evolutionary processes were important since the origin of replication. However, major transitions in the evolution like the origin of eukaryotes could be brought about by (effectively) unique events such as endosymbiosis, and the earliest stages of evolution (pre-LUCA) partially relied on distinct processes not involved in subsequent, “normal” evolution.

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The 3 modalities of evolution

Koonin, Wolf, Biol. Direct 2009

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NATURE REVIEWS| MICROBIOLOGY VOLUME 9 | JUNE 2011 | 46

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Makarova et al. Nature Rev Microbiol 2011

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CRISPR/Cas: a case of bona fide Lamarckian evolution

Koonin, Wolf, Biol. Direct 2009…although elements of stochasticity and selection are always present

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ionMali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM.

RNA-guided human genome engineering via Cas9. Science. 2013 Feb

15;339(6121):823-6.

Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F. Multiplex genome engineering using CRISPR/Cas systems.Science. 2013 Feb 15;339(6121):819-23

Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012 Aug 17;337(6096):816-21

Brouns SJ. Molecular biology. A Swiss army knife of immunity. Science. 2012 Aug 17;337(6096):808-9

Lamarck’s gift to biotechnology

Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013 Nov;8(11):2281-308

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Phenomenon Biological role/function Phyletic spread Lamarckian criteria

Genomic changes caused by environmental factor

Changes are specific to relevant genomic loci

Changes provide adaptation to the causative factor

Bona fide LamarckianCRISPR/Cas Defense against viruses

and other mobile elementsMost of the Archaea and many bacteria

Yes Yes Yes

piRNA Defense against transposable elements in germline

Animals Yes Yes Yes

HGT (specific cases)

Adaptation to new environment, stress response, resistance

Archaea, bacteria, unicellular eukaryotes

Yes Yes Yes

Quasi-LamarckianHGT (general phenomenon)

Diverse innovations Archaea, bacteria, unicellular eukaryotes

Yes No Yes/no

Stress-induced mutagenesis

Stress response/resistance/adaptation to new conditions

Ubiquitous Yes No or partially

Yes (but general evolvability enhanced as well)

Diverse Lamarckian and quasi-Lamarckian phenomena

Koonin, Wolf, Biol. Direct 2009

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Postmodern reassessment of some central propositions of Darwin and the Modern Synthesis

Proposition Postmodern status

The material for evolution is provided, primarily, by random, heritable variation.

Only partly true. The repertoire of relevant random changes greatly expanded to include duplication of genes, genome regions, and entire genomes; loss of genes and, generally, genetic material; HGT including massive gene flux in cases of endosymbiosis; invasion of mobile selfish elements and recruitment of sequences from them; and more. More importantly, (quasi)directed (Lamarckian) variation is recognized as a major factor of evolution.

The variations fixed by natural selection are “infinitesimally small”. Evolution strictly adheres to gradualism.

False. Even single gene duplications and HGT of single genes are by no means “infinitesimally small” let alone deletion or acquisition of larger regions, genome rearrangements, whole-genome duplication, and most dramatically, endosymbiosis. Gradualism is not the principal regime of evolution.

Uniformitarianism: evolutionary processes remained, largely, the same throughout the evolution of life.

Only partly true. Present day evolutionary processes were important since the origin of replication. However, major transitions in the evolution like the origin of eukaryotes could be brought about by (effectively) unique events such as endosymbiosis, and the earliest stages of evolution (pre-LUCA) partially relied on distinct processes not involved in subsequent, “normal” evolution.

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338 Archaea and Bacteria

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44 Escherichia and Salmonella

Cloud:~24000

Shell: ~5700Core:~70

Fractal (self-similar) structure of the prokaryotic gene space - Tripartite organizationof pangenomes at all levels – major differences in gene repertoires

Core genome

Accessory genome

Koonin, Logic of Chance 2011

The recurrent structure in the gene universe reflects dramatic genomeplasticity – extensive loss and gain of genes - at all levels

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PARADIGM SHIFT: from GENOMES TO PANGENOMES1960-1990

16S RNA

1990-2010

Genomes

2010-2020

Pangenomes

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Open (unlimited growth) vs closed pan-genome

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Mathematical modeling of pangenome evolution reveals closed pangenomes and exponential growth of estimated pangenome

size with tree depth

(Only) a million proteins for molecular biologists?

Lobkovsky, Wolf, Koonin, in preparation

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Postmodern reassessment of some central propositions of Darwin and the Modern Synthesis

Proposition Postmodern status

The material for evolution is provided, primarily, by random, heritable variation.

Only partly true. The repertoire of relevant random changes greatly expanded to include duplication of genes, genome regions, and entire genomes; loss of genes and, generally, genetic material; HGT including massive gene flux in cases of endosymbiosis; invasion of mobile selfish elements and recruitment of sequences from them; and more. More importantly, (quasi)directed (Lamarckian) variation is recognized as a major factor of evolution.

The variations fixed by natural selection are “infinitesimally small”. Evolution adheres to gradualism.

False. Even single gene duplications and HGT of single genes are by no means “infinitesimally small” let alone deletion or acquisition of larger regions, genome rearrangements, whole-genome duplication, and most dramatically, endosymbiosis. Gradualism is not the principal regime of evolution.

Fixation of (rare) beneficial changes by natural selection is the main driving force of evolution.

True only to a small extent. Natural (positive) selection is important but is only one of several fundamental factors of evolution and is not quantitatively dominant. Neutral processes combined with purifying selection dominate evolution, and direct effects of environmental cues on the genome - (quasi)Lamarckian phenomena - are important as well. Universal patterns of evolution seem to emerge without natural selection

Uniformitarianism: evolutionary processes remained, largely, the same throughout the evolution of life.

Only partly true. Present day evolutionary processes were important since the origin of replication. However, major transitions in the evolution like the origin of eukaryotes could be brought about by (effectively) unique events such as endosymbiosis, and the earliest stages of evolution (pre-LUCA) partially relied on distinct processes not involved in subsequent, “normal” evolution.

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The 3 modalities of evolution

Koonin, Wolf, Biol. Direct 2009

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fitne

ss

Selection and drift in classic population genetics

Selection - large Ne

drift+selection – small Ne

Sewall Wright (1889-1988)

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Non-adaptive evolution of genomic complexityNothing makes sense in evolution except in light of population genetics Lynch M. The frailty of adaptive hypotheses for the origins of organismal complexity. Proc Natl Acad Sci U S A. 2007

Lynch M, Conery JS. The origins of genome complexity. Science. 2003 Nov 21;302(5649):1401-4. Complete genomic sequences from diverse phylogenetic lineages reveal notable increases in genome complexity from prokaryotes to multicellular eukaryotes. The changes include gradual increases in gene number, resulting from the retention of duplicate genes, and More abrupt increases in the abundance of spliceosomal introns and mobile genetic elements. We argue that many of these modifications emerged passively in response to the long-term population-size reductions that accompanied increases in organism size. According to this model, much of the restructuring of eukaryotic genomes was initiated by nonadaptive processes, and this in turn provided novel substrates for the secondary evolution of phenotypic complexity by natural selection. The enormous long-term effective population sizes of prokaryotes may impose a substantial barrier to the evolution of complex genomes and morphologies.

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Estimates of the composite parameter Neu for a phylogenetically diverse assemblage of species

M Lynch, J S Conery Science 2003;302:1401-1404Published by AAAS

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The major intrusion of stochasticity into Biology: do statistical laws rule Life?

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Some key universals of genome/molecular phenome evolution

Karev et al. 2002; Jordan et al. 2004; Lobkovsky, Wolf, Koonin, 2010; Koonin, Wolf 2010

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PLoS Comput Biol. 2011 Aug;7(8):e1002173.

Are there laws of genome evolution?Koonin EV.Research in quantitative evolutionary genomics and systems biology led to the discovery of several universal regularities connecting genomic and molecular phenomic variables. These universals include the log-normal distribution of the evolutionary rates of orthologous genes; the power law-like distributions of paralogous family size and node degree in various biological networks; the negative correlation between a gene's sequence evolution rate and expression level; and differential scaling of functional classes of genes with genome size.

The universals of genome evolution can be accounted for by simple mathematical models similar to those used in statistical physics, such as the birth-death-innovation model. These models do not explicitly incorporate selection; therefore, the observed universal regularities do not appear to be shaped by selection but rather are emergent properties of gene ensembles. Although a complete physical theory of evolutionary biology is inconceivable, the universals of genome evolution might qualify as "laws of evolutionary genomics“ in the same sense "law" is understood in modern physics.

The major intrusion of stochasticity into Biology: do statistical laws rule Life?

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Laws and generative models in evolutionary genomics

Koonin, PLOS Comp Biol 2011

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Shannon entropy: H= -Spilogpi

Max(H) – most random, least unexpected distributionMaxEnt Principle: the probability distribution of any variable ina large ensemble of data/measurements tends to the distributionwith Max(H) within the applicable constraints

A general physical principle behind all universals?

Frank SA. The common patterns of natureJ Evol Biol. 2009; 22:1563-85Karev, Koonin: Parabolic Replicator Dynamicsand the Principle of Minimum Tsallis Information Gain. Biology Direct 2013The results of this analysis show that the general MaxEnt principle is the underlying law for the evolution of a broad class of replicator systems including not only exponential but also parabolic and hyperbolic systems. E. T. Jaynes

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Postmodern reassessment of some central propositions of Darwin and the Modern Synthesis

Proposition Postmodern status

The material for evolution is provided, primarily, by random, heritable variation.

Only partly true. The repertoire of relevant random changes greatly expanded to include duplication of genes, genome regions, and entire genomes; loss of genes and, generally, genetic material; HGT including massive gene flux in cases of endosymbiosis; invasion of mobile selfish elements and recruitment of sequences from them; and more. More importantly, (quasi)directed (Lamarckian) variation is recognized as a major factor of evolution.

Fixation of (rare) beneficial changes by natural selection is the main driving force of evolution.

Only partly true. Natural (positive) selection is important but is only one of several fundamental factors of evolution and is not quantitatively dominant. Neutral processes combined with purifying selection dominate evolution, and direct effects of environmental cues on the genome {(quasi)Lamarckian phenomena] are important as well.

The variations fixed by natural selection are “infinitesimally small”. Evolution adheres to gradualism.

False. Even single gene duplications and HGT of single genes are by no means “infinitesimally small” let alone deletion or acquisition of larger regions, genome rearrangements, whole-genome duplication, and most dramatically, endosymbiosis. Gradualism is not the principal regime of evolution.

Uniformitarianism: evolutionary processes remained, largely, the same throughout the evolution of life.

Only partly true. Present day evolutionary processes were important since the origin of replication. However, major transitions in the evolution like the origin of eukaryotes could be brought about by (effectively) unique events such as endosymbiosis, and the earliest stages of evolution (pre-LUCA) partially relied on distinct processes not involved in subsequent, “normal” evolution.

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“Amitochondrial” eukaryotes

“In the mid-1990s, a somewhat pedestrian view of eukaryotic origins, the 'archezoa hypothesis', held sway. This maintained that a protoeukaryote (with nucleus) engulfed the mitochondrial ancestor. Supporting the theory were 'archezoa', anaerobic eukaryotes with no mitochondria. Archezoa apparently populated the oldest branches of the eukaryote tree, suggesting that eukaryotes began diversifying before mitochondria entered the picture.”

Poole, Penny, Nature 447, 913 (21 June 2007)

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Animal mitochondrionHydrogenosome from an anaerobic fungus

Mitosomes from Giardia

There are no (known) true amitochondrial eukaryotes

Van der Giezen, Tovar. Degenerate mitochondria. EMBO Rep. 2005 Jun;6(6):525-30.

All “archezoa” possess:-mitochondrial genes in nuclear genomes-degenerate derivatives of mitochondriaThey are not archezoa at all!

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Hypotheses on the origin of eukaryotesEmbley, Martin, Nature 2006

????

“Archezoan” hypotheses “Symbiotic” hypotheses

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Martin, Koonin, 2006, Introns and the origin of nucleus-cytosol compartmentalization. Nature 440: 41-5

2 prokaryotes: archaeonand a-proteobacterium

Invasion

Unidirectional flow of genesand introns from symbiont tohost – ratchet due to propagation/lysis of symbiont

Dispersal of introns, population bottleneck

Origin of nucleus andspliceosome

Adaptation to survive the intron invasion

Non-adaptive process –Attack on the host genome

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The proposed chain of causes and effects in eukaryogenesis – the pivotal roles of mitochondrial endosymbiosis and intron invasion

Koonin, The origin of introns and their role in eukaryogenesis: a compromise solution to the introns-early versus introns-late debate? Biol Direct. 2006 Aug 14;1:22

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Proposition Postmodern status

Evolution by natural selection tends to produce increasingly complex adaptive features of organisms; hence progress as a general trend in evolution.

False. Genomic complexity probably evolved as a “genomic syndrome” caused by weak purifying selection in small population and not as an adaptation. There is no consistent trend towards increasing complexity in evolution, and the notion of evolutionary progress is unwarranted.

The entire evolution of life can be depicted as a single “big tree”.

False. The discovery of the fundamental contributions of HGT and mobile genetic elements to genome evolution invalidate the TOL concept in its original sense. However, trees remain essential templates to represent evolution of individual genes and many phases of evolution in groups of relatively close organisms. The possibility of salvaging the TOL as a central trend of evolution remains.

All extant cellular life forms descend from very few, and probably, one ancestral form (LUCA).

True. Comparative genomics leaves no doubt of the common ancestry of cellular life. However, it also yields indications that LUCA(S) might have been very different from modern cells.

Postmodern reassessment of some central propositions of Darwin and the Modern Synthesis

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Non-adaptive evolution of genomic complexityNothing makes sense in evolution except in light of population genetics Lynch M. The frailty of adaptive hypotheses for the origins of organismal complexity. Proc Natl Acad Sci U S A. 2007

Lynch M, Conery JS. The origins of genome complexity. Science. 2003 Nov 21;302(5649):1401-4. Complete genomic sequences from diverse phylogenetic lineages reveal notable increases in genome complexity from prokaryotes to multicellular eukaryotes. The changes include gradual increases in gene number, resulting from the retention of duplicate genes, and More abrupt increases in the abundance of spliceosomal introns and mobile genetic elements. We argue that many of these modifications emerged passively in response to the long-term population-size reductions that accompanied increases in organism size. According to this model, much of the restructuring of eukaryotic genomes was initiated by nonadaptive processes, and this in turn provided novel substrates for the secondary evolution of phenotypic complexity by natural selection. The enormous long-term effective population sizes of prokaryotes may impose a substantial barrier to the evolution of complex genomes and morphologies.

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There is no general trend toward increasing complexity in evolution…actually, the opposite might be true

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Reconstruction of archaeal genome evolution: reduction prevails

Wolf YI, Makarova KS, Yutin N, Koonin EV. Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer. Biol Direct. 2012 Dec 14;7:46

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Maximum Likelihood (MCMC) reconstruction of intron gain/loss during eukaryote evolution from comparative-genomic analysis of 100 genomes (mean/median+ confidence intervals)• Pronounced excess of loss over gain: mostly a story of decreasing complexity• Intron-rich ancestors • Human-like intron-density in Last Eukaryotic Common Ancestor (LECA)• No intron-poor stage from LECA to mammals – no stage of intense purifying selection

Csuros, Rogozin Koonin, PLOS Comp Biol 2011

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time

log

com

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ity

Punctuated model of evolution: long phases of reduction punctuated by bursts

Wolf, Koonin, BioEssays 2013

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Proposition Postmodern status

Evolution by natural selection tends to produce increasingly complex adaptive features of organisms; hence progress as a general trend in evolution.

False. Genomic complexity probably evolved as a “genomic syndrome” caused by weak purifying selection in small population and not as an adaptation. There is no consistent trend towards increasing complexity in evolution, and the notion of evolutionary progress is unwarranted.

The entire evolution of life can be depicted as a single “big tree”.

False. The discovery of the fundamental contributions of HGT and mobile genetic elements to genome evolution invalidate the TOL concept in its original sense. However, trees remain essential templates to represent evolution of individual genes and many phases of evolution in groups of relatively close organisms. The possibility of salvaging the TOL as a central trend of evolution remains.

All extant cellular life forms descend from very few, and probably, one ancestral form (LUCA).

True. Comparative genomics leaves no doubt of the common ancestry of cellular life. However, it also yields indications that LUCA(S) might have been very different from modern cells.

Postmodern reassessment of some central propositions of Darwin and the Modern Synthesis

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Thinking of the history of life in terms of phylogenetic trees is as old as scientific biology (if not older)

Charles Darwin (1859) Origin of Species [one and only illustration]: "descent with modification"

Ernst Haeckel (1879)The Evolution of Man

A brief history of TOL

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Advent of molecular phylogenetics – expectations of objectively reconstructed complete Tree of Life

Woese et al. (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. PNAS 87, 4576-4579 [Figure 1, modified]

A brief history of TOL

Carl R. Woese (1928-2012)

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“Forest of Life” to replace Tree of LifePuigbò P, Wolf YI, Koonin EV. Search for a 'Tree of Life' in the thicket of the phylogenetic forest. J Biol. 2009;8(6):59

-0.5

-0.4

-0.3

-0.2

-0.1

0

0.1

0.2

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-0.6 -0.4 -0.2 0 0.2 0.4 0.6 0.8

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NUTs

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Dr DsDr = 0.67 Ds > Dr

d’ =0 d’=1d’ = (d-Dr) / (Ds-Dr)

Ds DrDs < Dr Dr = 0.67

d’=1 d’=0d’ = 1 – ((d-Ds) / (Dr-Ds))

NUTs

FOL

0.63 +/- 0.35

0.39 +/- 0.31

TNT (Tree/Net Trend): scoring tree-like and net-like evolution quantitatively

0: Network(green) – Neutral (black) – 1:Tree (red) Puigbo, Wolf, Koonin, Genome Biol Evol 2010

Horizontal gene flow dominatesevolution, at least in prokaryotes

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Proposition Postmodern status

Evolution by natural selection tends to produce increasingly complex adaptive features of organisms; hence progress as a general trend in evolution.

False. Genomic complexity probably evolved as a “genomic syndrome” caused by weak purifying selection in small population and not as an adaptation. There is no consistent trend towards increasing complexity in evolution, and the notion of evolutionary progress is unwarranted.

The entire evolution of life can be depicted as a single “big tree”.

False. The discovery of the fundamental contributions of HGT and mobile genetic elements to genome evolution invalidate the TOL concept in its original sense. However, trees remain essential templates to represent evolution of individual genes and many phases of evolution in groups of relatively close organisms. The possibility of salvaging the TOL as a central trend of evolution remains.

All extant cellular life forms descend from very few, and probably, one ancestral form (LUCA).

True. Comparative genomics leaves no doubt of the common ancestry of cellular life. However, it also yields indications that LUCA(S) might have been very different from modern cells.

Postmodern reassessment of some central propositions of Darwin and the Modern Synthesis

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~100 universally conserved protein and RNA genes =primarily translation system components

LUCA: undeniable but elusive

Koonin EV. Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat Rev Microbiol. 2003

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Mulkidjanian AY, Bychkov AY, Dibrova DV, Galperin MY, Koonin EV. Origin of first cells at terrestrial, anoxic geothermal fields. Proc Natl Acad Sci U S A. 2012 Apr 3;109(14):E821-30

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rand

om

det

erm

ini

stic

generation of variationrandom

deterministic

fixation of variation/mode of genome evolution

drift

draft

direct adaptation

strong selection

weak selection

intermediate selection

CRISPR spacer acquisition

resistance plasmid acquisition

horizontal gene transfer

stress-induced mutagenesis

transposition-induced shufflinggene duplication

gene lossrandom mutation

genomestreamlining

degradation ratchet

Junkaccumulation/complexification

From randomness to determinism: evolution spans the whole range

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The biosphere as the world of viruses

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• Viruses are the most abundant biological entities in the biosphere: there are 10-100 virus particles per cell• The pangenomes of viruses and cellular organismshave [at least] comparable complexities

1 cm3 of seawater contains 106-109 virus particles

There are millions of diverse bacteriophage speciesin the water, soil, and gut

Suttle, C.A. (2005) Nature 437:356

Edwards and Rohwer (2005) Nat. Rev. Microbiol. 3:504

Viruses are the dominant entities in the biosphere – physically and genetically – as shown by viral metagenomics – virome studies

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Some of the largest viruses host their own parasites

La Scola et al. The virophage as a unique parasite of the giant mimivirus.Nature. 2008 Sep 4;455(7209):100-4

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Philippe et al. Pandoraviruses: Amoeba Viruses with Genomes Up to 2.5 Mb Reaching That of Parasitic EukaryotesScience 19 July 2013: Vol. 341 no. 6143 pp. 281-286

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(At least) two independent origins of giant viruses: Pandoraviruses appear to be highly derived Phycodnaviruses

Mimi

Pandora

Smaller,simpler commonancestor(?)

Yutin, Koonin.Biol. Direct 2013

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• Viruses and virus-like genetic elements are not “just” pathogens: they are dominant entities in the biosphere

• Emergence of virus-like parasites is inevitable in any replicating system• In the pre-cellular epoch, the genetic elements that later became viral and cellular

genomes comprised a single pool in which they mixed, matched, and evolved new, increasingly complex gene ensembles

• Different replication strategies including RNA replication, reverse transcription,and DNA replication evolved already in the primordial genetic pool• With the emergence of prokaryotic cells, a distinct pool of viral genes formed that

retained its identity ever since as evidenced by the extant distribution ofviral hallmark genes: “virus world” or the virosphere• The emergence of the eukaryotic cell was a second melting pot of virus evolution, from

which viruses of eukaryotes originated via recombination of genes from prokaryote viruses, retroelements, and the evolving eukaryotic host

• Viruses make essential contributions to the evolution of the genomes of cellularlife forms, in particular, as vehicles of HGT: GTAs, transducing phages

The ancient Virus World

Koonin EV, Senkevich TG, Dolja VV. The ancient Virus World and evolution of cells. Biol Direct. 2006

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dsDNA viruses

ssDNA viruses

dsRNA viruses

(+)RNA viruses

(-)RNA viruses

viroids

Retroviruses/elements

Bacteria

Eukaryota

Archaea

Virus Empire Cellular Empire

Koonin, Logic of Chance 2011

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Darwinian theory of natural selection

Population geneticsQuantitative theory of selection

and drift

Neutral theory

Selfish gene

HG

T

ph

ylo

ge

no

mic

s

Neo-Lamarckian evolution models

Lamarckian L'influence des circonstances

constructive neutral evolution of complexity

evo

lutio

n

of

evo

lva

bili

ty

Modified from: Koonin EV, Wolf YI. Evolution of microbes and viruses: a paradigm shift in evolutionary biology? Front Cell Infect Microbiol. 2012;2:119

Virus World

Quantitative laws and physical

principles of evolution

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FT Press; 1 edition (September 10, 2011)Marine Corps marathon 2011,Washington, DC

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Acknowledgments

Bill Martin Valerian Dolja Didier Raoult